46(913):71–87
Spermophilus citellus (Rodentia: Sciuridae)
NICOLÁS RAMOS-LARA, JOHN L. KOPROWSKI, BORIS KRYŠTUFEK,
AND
ILSE E. HOFFMANN
School of Natural Resources and the Environment, 325 Biological Sciences East Building, University of Arizona, Tucson, AZ
85721, USA; ramosln@yahoo.com.mx (NRL); squirrel@ag.arizona.edu (JLK)
Slovenian Museum of Natural History, Prešernova 20, SI-1000 Ljubljana, Slovenia; boris.krystufek@zrs.upr.si (BK)
Department of Behavioural Biology, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria; ilse.hoffmann@univie.ac.at
(IEH)
Abstract: Spermophilus citellus (Linnaeus, 1766) is a medium-sized sciurid commonly called the European ground squirrel.
The species inhabits grasslands in central and southeastern Europe on a range from short-grass steppes to meadow orchards,
and from sea level to an elevation of 2,500 m. These squirrels live in colonies and construct burrows used for hibernation,
reproduction, refuge, and resting. Due to serious declines in many portions of its range, the species is listed as ‘‘Vulnerable’’ by
the International Union for Conservation of Nature and Natural Resources. It is also protected by the Bern Convention
(Appendix II), and the European Union Habitats and Species Directive (Annexes II and IV).
Key words:
Citellus citellus, endemic species, Europe, European ground squirrel, European souslik, suslik
Ó 12 December 2014 American Society of Mammalogists
Synonymy completed 25 September 2012
DOI: 10.1644/913.1
Spermophilus citellus (Linnaeus, 1766)
European Ground Squirrel
Mus citellus Linnaeus, 1766:80. Type locality ‘‘Austria,
Bohemia, Polonia,’’ restricted to Austria by Miller
(1912:924); restricted to Wagram, Austria, by Martino
and Martino (1940:496).
Mus citillus Pallas, 1779:119. Incorrect subsequent spelling
of Mus citellus Linnaeus, 1766.
Spermophilus citellus: Cuvier, 1825:255. First use of current
name combination.
Citellus citellus gradojevici Martino and Martino, 1929:76.
Type locality ‘‘Djerdjelija [¼ Gevgelija], Macedonia.’’
Citellus citellus istricus Calinescu, 1934:106. Type locality
‘‘Ebene Munteniens [¼ lowlands of Muntenia],’’ southeastern Romania.
Citellus citellus karamani Martino and Martino, 1940:495.
Type locality ‘‘Karadjica [¼ Mt. Karadžica] Mountains,
above Patiška, 30 km south of Skoplje [¼ Skopje],
southern Serbia,’’ Macedonia.
Citellus citellus laskarevi Martino and Martino, 1940:498.
Type locality ‘‘Dolovo, southeastern Banat, Yugoslavia,’’ Serbia.
Citellus citellus martinoi Peshev, 1955:290. Type locality
‘‘Rodopite, okolnostite na v. Kolarov (Belmeken),’’ (¼
Rhodopen Mts., neighborhoods of the peak Kolarov
[Belmeken]), Bulgaria.
Citellus citellus balcanicus Markov, 1957:465. Type locality
‘‘Okolnostite na s. Lokorsko, Sofijsko, na ûg ot
www.mammalogy.org
Balkana, Blgariâ,’’ (¼ neighborhoods of the village
Lokorsko, region of Sofia, southern Balkan Mts.,
Bulgaria).
Citellus citellus thracius Mursaloğlu, 1964:260. Type locality
‘‘A valley-meadow in front of the south-east slope of
Murattepe, near Yenibedir, Lüleburgaz, Kirklareli,
Turkey in Europe.’’
Fig. 1.—An adult Spermophilus citellus from Mladá Boleslav,
Czech Republic. Photograph courtesy of A. Kryštufek.
MAMMALIAN SPECIES
72
Citellus citellus macedonicus Fraguedakis-Tsolis, 1977:65.
Type locality ‘‘Kozani;’’ restricted to Pontokomi,
Kozani, West Macedonia, Greece, by FraguedakisTsolis and Ondrias (1985:196).
CONTEXT AND CONTENT. Order Rodentia, suborder Sciuromorpha, family Sciuridae, subfamily Xerinae, tribe Marmotini, genus Spermophilus (Helgen et al. 2009).
Designation of subspecies for S. citellus has been contentious. Eight subspecies have been described since 1929 based
on slight differences in color, size, and body proportions
(Ružić 1978), but with no proof of discontinuity (Corbet
1978). Ružić (1978) tentatively recognized 7 subspecies (all,
except balcanicus, which she synonymized with martinoi),
whereas other authors have recognized only 4 subspecies
(Thorington and Hoffmann 2005; Thorington et al. 2012):
citellus, gradojevici (karamani is a synonym), istricus
(laskarevi is a synonym), and martinoi (balcanicus and
thracius are synonyms). Skull characters, ratios, and
coloration are of low diagnostic value in S. citellus and the
above subspecies were not consistent with the interlocality
variation observed in an analysis of 13 cranial measurements
of ground squirrels from throughout the range (Kryštufek
1996), suggesting that further revision of the subspecies is
needed.
NOMENCLATURAL NOTES. The name Citellus (Oken, 1816)
was in routine use for the genus until Hershkovitz (1949)
argued that Oken’s work was invalid, and that Spermophilus
(Cuvier, 1825) was the oldest available name for the genus.
The opinion was supported by the International Commission on Zoological Nomenclature (1956; Opinion 417), and
has been adopted by American authors. However, some
European and Russian authors continued to use Citellus as
recently as 1995, although others adopted Spermophilus
(Harrison et al. 2003). Until recently, Spermophilus contained all Holarctic ground squirrels, except those in the
genera Marmota, Cynomys, and Ammospermophilus and was
further divided into 6 subgenera. Presently, Spermophilus
contains 14 species (sensu lato), all restricted to Eurasia
(Helgen et al. 2009). Spermophilus is derived from the Greek
spermatos for seed and phileo for love (Helgen et al. 2009),
whereas citellus is from the Latin ziesel (German for ground
squirrel or souslik—Palmer 1904). S. citellus also has been
referred to as the European souslik (Coroiu et al. 2008).
DIAGNOSIS
Spermophilus citellus together with S. xanthoprymnus
(Asia Minor ground squirrel), S. dauricus (Daurian ground
squirrel), S. suslicus (speckled ground squirrel), S. alashanicus (Alashan ground squirrel), and S. taurensis (Taurus
ground squirrel) form a group of closely related species, so
that single specimens are sometimes indistinguishable;
46(913)—Spermophilus citellus
however, their distributions are different (Vinogradov and
Argiropulo 1941; Herron et al. 2004; Gündüz et al. 2007;
Helgen et al. 2009). Compared to S. taurensis, diagnostic
characters for S. citellus are as follows: less reddish dorsal
pelage, underside more yellow, smaller body size (S.
taurensis, range: 194–201 mm; S. citellus, range: 174–228
mm), tail slightly longer (S. taurensis, range: 62–65 mm; S.
citellus, range: 31–90 mm) with a dark stripe along its dorsal
side, and hind-foot length shorter (S. taurensis, range: 39–44
mm; S. citellus, range: 30–43 mm—Kryštufek and Vohralı́k
2005, 2012; Gündüz et al. 2007; Özkurt et al. 2007).
Compared to S. xanthoprymnus (see Gür and Gür 2010),
diagnostic characters for S. citellus are as follows: the skull
is less angular, back indistinctly spotted, and tail longer (S.
xanthoprymnus, range: 30–72 mm; S. citellus, range: 31–90
mm) with black hairs dorsally (Kryštufek and Vohralı́k
2005, 2012). S. citellus, S. taurensis, and S. xanthoprymnus
can be clearly distinguished on the basis of their alarm calls
(Schneiderová and Policht 2011a, 2011b).
GENERAL CHARACTERS
Spermophilus citellus is a medium-sized ground squirrel,
with a round body, short tail (20–40% of length of head and
body), and reduced outer ears (Fig. 1). Head is convex in
profile with large eyes (about 8 mm in diameter) and short
vibrissae (25–30 mm—Ružić 1978; Kryštufek and Vohralı́k
2005). The eyes, situated wide apart on the upper side of
head, present an ill-defined eye-ring, whitish or yellowish
according to general coloring of body (Miller 1912; Ružić
1978). The tail is cylindrical at the base and inconspicuously
flattened beyond the middle, where hairs are about 15 mm
long. The tail lacks a definite color pattern, with the upper
surface grizzled, essentially like the back, somewhat darker
at tip, and the pencil with light margin; the undersurface is a
nearly clear dull buff. The ears are low, obscurely pointed
above, and densely covered with fine, short hairs on both
surfaces but without tufts (Miller 1912; Kryštufek and
Vohralı́k 2005). The back and sides of the body are usually
cream-buff but occasionally more yellowish, with sides
inconspicuously lined with black, the entire dorsal surface
from nape to rump vermiculated with black, and the dark
and light areas along the middle of the back usually well
enough defined to produce an effect of obscure light
mottling, with spots about 5 mm in diameter. The belly is
washed with a buff usually somewhat more yellow than that
of sides. The crown and upper half of cheeks are grizzled,
with the light element paler than on the body and the dark
relatively more evident, the muzzle sometimes with a rusty
tinge, and the sides of muzzle and lower half of cheeks clear
whitish or buffy, continuous with the similarly colored pale
area covering throat and forepart of chest and inner side of
foreleg (Miller 1912). Feet are yellowish, with longest claws
up to 8 mm in length, and 4 fairly large and naked pads on
46(913)—Spermophilus citellus
MAMMALIAN SPECIES
palms and soles; rudimentary thumbs still bear a nail
(Kryštufek and Vohralı́k 2005). Soles are covered with short
silvery hairs from heel to pads (Calinescu 1934; Kryštufek
and Vohralı́k 2012). In 2012, a light-colored morph was
detected in Vienna, Austria, with white tail and belly, and
interspersed white blotches on head and dorsum (n . 5—I.
E. Hoffmann, in litt.).
Size and body mass of S. citellus vary with age, sex, and
activity cycle, but also with locality and environmental
conditions (Ružić 1978; Hoffmann et al. 2008; Millesi and
Hoffmann 2008). Male-biased sexual dimorphism develops
during the juvenile summer (Millesi et al. 1999b) and
increases with age (Ružić 1978: table 15; Spitzenberger and
Bauer 2001). Mean body mass of Pannonian juveniles at 30
days of age was 61.4 g (Ružić 1965). Data from an Austrian
population ranged between , 50 g (juveniles at emergence
from their natal burrow) and . 450 g ( 1-year-old males
prior to hibernation). At vernal emergence, males were
heavier than females in the same age class, and adult animals
were heavier than yearlings. Adult males attained a
minimum annual mass during the mating phase (Millesi et
al. 1999b), whereas yearling males and females weighed least
at emergence from hibernation (Millesi et al. 1998; Millesi
and Hoffmann 2008). Growth of hind feet may terminate in
juveniles, whereas head length still increases during the 2nd
year (Ružić 1978; Millesi et al. 1999a).
Ranges of external measurements (mm) for adult ( 1
year old) S. citellus were: length of head and body, males:
176–228, females: 174–217; length of tail, males: 31–90,
females: 38–75; length of hind foot, males: 32–43, females:
30–41; length of ear, males: 6.0–15.4, females: 6.7–12.2; and
body mass, males: 125–380 g, females: 131–353 g (Miller
1912; Ružić 1978; Spitzenberger and Bauer 2001; Kryštufek
and Vohralı́k 2005). In spite of geographic heterogeneity
observed in 13 cranial measurements (Kryštufek 1996),
sexual dimorphism in cranial size is apparently fairly
constant across the species’ range (Kryštufek and Vohralı́k
2012). Mean (mm – SE) cranial measurements from Austria
and Hungary (n ¼ 27), Romania (n ¼ 8), Bulgaria (n ¼ 3),
and Turkey (n ¼ 1) were: condylobasal length, 43.11 – 1.15;
zygomatic breadth, 28.84 – 0.59; breadth of rostrum at
front of nasals, 7.62 – 0.29; interorbital breadth, 9.60 –
0.30; postorbital breadth, 11.78 – 0.54; mastoid breadth,
20.24 – 0.60; occipital depth, 12.96 – 0.48; length of nasals,
14.60 – 4.89; length of diastema, 11.82 – 0.33; length of
mandible, 29.95 – 0.63; length of maxillary toothrow, 9.73
– 0.37; and length of mandibular toothrow, 9.49 – 0.33
(Fig. 2; Miller 1912).
Baculum varies geographically, with its spoonlike
expanded distal spatula triangular, and with toothlike
projections along its ventral margin (Kryštufek and
Vohralı́k 2005). The baculum is asymmetrical, most clearly
in the shape of the spatula. Mean measurements (mm) of 35
bacula from the Czech Republic (n ¼ 2), Serbia (n ¼ 18), and
73
Fig. 2.—Dorsal, ventral, and lateral views of skull and lateral view
of mandible of an adult male Spermophilus citellus (Slovenian
Museum of Natural History 7082) from Samoš, Deliblato Sands,
Voivodina, Serbia. Greatest length of skull is 42.7 mm.
Photographs by C. Mlinar used with permission.
MAMMALIAN SPECIES
74
46(913)—Spermophilus citellus
FOSSIL RECORD
The genus Spermophilus (sensu lato) is known in Europe
from the late Miocene and Spermophilus citellus appears in
the middle Pleistocene when known in Bulgaria, Greece,
Hungary, and Romania (Kowalski 2001). Examination of
paleontological data suggests that ground squirrels manifest
morphological variability from the early Pleistocene through
the present and the evolution of S. citellus apparently
occurred mainly in the Balkans (Peshev et al. 2004). The
species apparently has been confined to its current range
since its earliest appearance in the fossil record (Kryštufek et
al. 2009). No fossils of S. citellus are known from Austria
(Spitzenberger and Bauer 2001).
FORM AND FUNCTION
Fig. 3.—Geographic distribution of Spermophilus citellus. The red
triangle shows the area where the species has been successfully
reintroduced in Poland. Map created by N. Ramos-Lara based on
Coroiu et al. (2008).
Macedonia (n ¼ 15) were: length of baculum, 2.5–3.2; basal
breadth, 0.9–1.2; spatula breadth, 1.1–1.6; and number of
denticles, 8.7–13.0 (Kryštufek and Hrabě 1996).
DISTRIBUTION
Endemic to central and southeastern Europe, between
40820 0 N and 51800 0 N and 12840 0 E and 29800 0 E (Fig. 3;
Ružić 1978), the range of Spermophilus citellus is disjunct,
the Carpathians and the Djerdap Canyon of the Danube
divide the range into 2 portions. The northwestern portion
extends through the lowlands of the Czech Republic,
Austria, Hungary, Slovakia, Serbia (to the north of
Danube and Sava), and eastern Romania. The southeastern portion extends from eastern Serbia, Macedonia, and
northern Greece through Bulgaria to Turkish Thrace,
southern and eastern Romania, Moldova, and Ukraine
(Kryštufek 1999; Kryštufek and Vohralı́k 2005; Coroiu et
al. 2008). Extinct in Germany, Poland, and Croatia, the
western margin of its distribution is in the Czech Republic
(Coroiu et al. 2008; Hulová and Sedláček 2008). Nonetheless, the species was successfully reintroduced in Poland
(Fig. 3; Coroiu et al. 2008; Matějů et al. 2010b). Evidence
suggests that S. citellus started to spread across its recent
distribution 5,000 years ago, after Neolithic deforestation
(Spitzenberger and Bauer 2001). Knowledge of the
distribution in the southern portion of its range remains
incomplete (Koshev 2008).
Form.—The skull of Spermophilus citellus is similar to
that of Sciurus but smaller (Kryštufek and Vohralı́k 2005).
The braincase is broadly ovate when viewed from above,
with greatest width equal to length, and its posterior width
exceeding that at the postorbital constriction (Miller 1912).
Dental formula is: i 1/1, c 0/0, p 2/1, m 3/3, total 22. P1 has 1
root; P2, M1, M2, and M3 have 3 roots; p1 has 2 roots; and
m1, m2, and m3 have 4 roots (Özkurt et al. 2007). Age of
individuals can be assessed through enamel abrasion of
dental material (Ružić 1966) and on the basis of layers of
appositional bone in the mandible (Hrabě and Zejda 1981).
Kry štufek (1998) found differences in 15 pelvic
measurements between localities and sexes. The characters
most affected by interlocality variation were those
describing general length and pelvis breadth, whereas
males attained higher average sample means in all
characters except breadth at pubic symphysis and pubis
width at symphysis. The number of mammae is: 1-1 p, 2-2 a,
2-2 i, total 10 (Miller 1912).
Spermophilus citellus has internal cheek pouches. The
paired retractor muscles attach dorsally to scapular metacromion and ventrally to sternum. These muscles are
presumably derived only from the facial musculature
(platysma myoides p. branchialis and musculus sphincter colli
profundus p. intermedia ventralis), rather than from musculus
trapezius p. auricularis, as is the case in other rodents
(Zherebtsova 2005).
The eye lens is yellow and does not transmit ultraviolet
radiation (50% cutoff around 493 nm—Hut et al. 2000). The
retinal photoreceptor mosaic is composed mainly of cones
and , 3% of the visual cells show rod-like characteristics
(Szél and Röhlich 1988). Half of the rod-like cells are
recognized solely by a rhodopsin antibody, whereas the
other half also are recognized by a blue opsin antibody
(Schantz et al. 1994). The species is dichromat having only
blue (440 nm) and green (520–525 nm) photopic spectral
46(913)—Spermophilus citellus
MAMMALIAN SPECIES
sensitivities, together with 1 scotopic component with an
absorption peak at about 500 nm (Szél and Röhlich 1988).
Similar to other burrowing mammals (Kley and Kearney
2007), the forelimb of S. citellus is characterized by welldeveloped scapular retractors, arm retractors with distal
insertions upon a robust humerus, elbow extensors and
flexors, forearm pronators with distal insertions, and carpal
and digital flexors with extensive origins from a prominent
medial humeral epicondyle (Lagaria and Youlatos 2006).
Three anal glands secrete an odorous scent that is
perceivable near burrow entrances, especially during the
mating season. Subcutaneous fat layer ranges from 2 to 5
mm in width (Ružić 1978).
Function.—During hibernation, Spermophilus citellus exhibits a regular pattern of torpor interrupted by euthermic
arousal phases (Strijkstra 1999). Evidence suggests that
animals interrupt torpor states regularly during hibernation
to protect the brain against the effects of prolonged
hypothermia (Ruediger et al. 2007). Memory retention in
captive S. citellus was negatively affected by hibernation.
The resulting memory loss is apparently related to the
physiological processes occurring during torpor and the
short euthermic phases (Millesi et al. 2001). Protein and
RNA contents in liver were higher during arousals than
during torpor. However, adrenal ascorbic acid concentration was less in aroused squirrels than in hibernating or
euthermic controls (Petrović et al. 1985).
Average euthermic body temperatures are highest after
hibernation and lowest during hibernation. Lowest body
temperatures during torpor may reach , 08C (Hut et al.
2002a). S. citellus shows reduction or absence of circadian
rhythmicity in body temperature for several days posthibernation, which may be due to the effects of prolonged periods
of extreme low body temperatures on the suprachiasmatic
nuclei (Hut et al. 2002b). Blood glucose concentrations in
captive S. citellus decreased substantially during hibernation, as in other hibernators, but hemoglobin levels
remained the same. Despite decreased liver metabolic
activity in captive hibernating animals, antioxidant defense
was maintained at a level comparable to that of animals in
the spring, or actually increased (Buzadžić et al. 1990).
Levels of the glucocorticoid hormone cortisol in captive
individuals varied seasonally in euthermic animals, being
higher from July to August than from April to May, and
most elevated from late October to December. In torpid
animals, blood cortisol levels also were low from October to
December and higher from January to March (Shivatcheva
et al. 1988). The levels of 17-hydroxycorticosteroids and free
amino acids in the plasma of aroused animals were higher
than those in hibernation and euthermic controls in captive
individuals (Petrović et al. 1985). Estradiol levels in freeliving S. citellus increase from proestrus to estrus among
females (Millesi et al. 2000). During late lactation, estradiol
levels also are considerably elevated, indicating initiation of
75
follicular maturation processes during that period (Huber et
al. 1999). After the termination of lactation, both estradiol
and progesterone secretion peak and decrease before
hibernation (Millesi et al. 2008). Females with high estrogen
titers produce larger litters the following year (Huber et al.
1999). Testosterone levels in mature males are high at the
beginning of aboveground activity and during mating, and
decrease thereafter. In nonreproductive yearling males,
androgen levels remain baseline throughout the active
season (Millesi et al. 1998; Strauss et al. 2007b).
ONTOGENY AND REPRODUCTION
Ontogeny.—Gestation period for Spermophilus citellus
was 25–26 days in captivity (Ružić 1978) and on average 29
days in the field (Millesi et al. 1999a; Aschauer et al. 2006),
with a positive correlation between gestation length and
litter size (Huber et al. 2001). In embryos of 10 mm in
length, the extraocular muscles were already developed as
independent bundles. At this stage, the attachment of the
musculature to the ocular wall was already distinctly
defined, with muscles fixed on the connective tissue
surrounding the eye. However, the final arrangement of
the musculature can be observed only after the embryo has
exceeded 2 cm in length, and the facial region of the head
has developed (Lešer 1925). External characters for 7
newborn specimens from European Turkey were: mean
total length, 57.18 mm; mean tail length, 7.75 mm; mean
hind-foot length, 7.50 mm; mean ear length, 1.00 mm; and
mean body mass, 5.25 g (Özkurt et al. 2005). The abdomens
of newborns were light pink, the backs of their bodies gray,
eyes and ears closed, and bodies hairless. Newborns became
hairy at 15–17 days, and eyes opened between 22 and 25
days. Between 25 and 27 days after birth upper and lower
incisors erupted, and ears opened on day 30 (Özkurt et al.
2005). Structural growth ceases at about 57 days of age,
which is probably related to gain of fat reserves for
hibernation (Millesi et al. 1999b). Sexes display similar
patterns of ontogenetic allometry and the majority of cranial
shape changes during growth probably are due to the shift
from liquid to solid diet (Klenovšek and Kryštufek 2013).
Juveniles 1st emerged from their burrows at 25 days of age
(Ružić 1965, 1978). Juveniles remain in their natal burrow
for about 1 month, and weaning begins in mid-June
depending on litter size and maternal condition (Millesi et
al. 1999a). Weaning occurs on average between 49.4 and
56.1 days, depending on litter size. Juvenile weaning body
mass is unaffected by litter size, although a trade-off exists
between litter size and juvenile body mass at natal
emergence (Huber et al. 2001). In Turkey, individuals born
between late April and early May reached adult size by
August and became reproductively active after 1 hibernation
period (Özkurt et al. 2005).
76
MAMMALIAN SPECIES
Reproduction.—Reproduction in Spermophilus citellus is
constrained by hibernation, limiting the timing of mating
and gonadal development (Huber et al. 1999). Females
deliver only 1 litter annually (Ružić 1978; Kryštufek and
Vohralı́k 2005), with litter sizes at emergence from natal
burrows ranging from 2 to 11 young/litter (Peshev 1955;
Pakizh 1958; Straka 1961; Ružić 1978; Millesi et al. 1999a;
Huber et al. 2001; Aschauer et al. 2006; Strauss et al. 2007a).
Litter size varies with latitude (Kryštufek and Vohralı́k
2005) and population density (Hoffmann et al. 2003a), with
southern and sparse populations having larger litters.
Consistency of litter size at natal emergence and in utero
(2–9 young/litter—Ružić 1978) suggests that the number of
offspring is determined prenatally, but whether the decision
is made preimplantation or later during pregnancy remains
unknown (Millesi et al. 1999a). In northern Serbia, the
proportion of nonreproductive females was very low (1.3%);
35.3% of pregnant females resorbed 1 or 2 embryos (RužićPetrov 1950). Large litters typically emerge early in the
season whereas small litters emerge later (Huber et al. 2001).
Although most females are sexually mature after their 1st
hibernation, the timing of puberty in males is facultative
(Millesi et al. 1998), becoming sexually active either as
yearlings or as 2 year olds (Millesi et al. 1999b). Testicular
condition is apparently predetermined before male
emergence, as adult males emerge with maximal testes size
(8.5–10 mm—Millesi et al. 1998) and elevated plasma
testosterone levels (Millesi et al. 2002). Early yearlings
with emergence masses . 220 g also present developed
testes, and display a pattern of testicular regression similar
to that of adults (Millesi et al. 1998). Male mating
opportunities are limited by availability of receptive
females, and gonadal regression starts at the end of the
mating period (Millesi et al. 2000, 2002), after the majority
of females have been impregnated. Females mate within 3
weeks after vernal emergence to give their offspring time to
grow and fatten before hibernation (Millesi et al. 1999a,
2000). In a free-ranging population in Austria, vaginal estrus
occurred 2–13 days after emergence from hibernation
(Millesi et al. 2000), with estrous dates ranging between 20
March and 19 April (Millesi at al. 1999a). Females with low
emergence mass show delayed estrus, resulting in smaller
and female-biased litters (Aschauer et al. 2006); early litters,
in contrast, are larger and male-biased (Millesi et al. 1999a).
Presence of males seems to have no effect on the latency to
go into vaginal estrus. However, in absence of males,
duration of vaginal estrus is lengthened by females (Millesi
et al. 2000). It is unknown whether S. citellus is a
spontaneous or induced ovulator (Millesi et al. 1998).
Mating can be a relatively long-lasting and costly event
for males. The average duration (mean – SD, n ¼ 12) of the
mating event is 0.7 – 0.3 h (Millesi et al. 1998). Copulation
occurs exclusively underground, but examination of
behavioral data suggests that each female mates only with
46(913)—Spermophilus citellus
a single male (Millesi et al. 1998). Copulatory plugs were not
detected in free-living adult females from Austria (Huber et
al. 2001).
Female S. citellus are monestrous; but there is growing
evidence for a 2nd nonreproductive estrous cycle in summer
(Millesi et al. 2008; Strauss et al. 2009). Follicular
development apparently is initiated during summer prior
to the hibernation period (Huber at al. 1999; Millesi et al.
2008; Strauss et al. 2009). The end of the follicular phase and
pregnancy are accompanied by luteal development (Millesi
et al. 2000). The ovaries of 36 captive squirrels were enlarged
in March, with vesicular follicles on the surface surrounded
by blood vessels. In April, the ovaries were further enlarged
due to the presence of corpus luteum, whereas in July their
sizes were greatly reduced (Tsvetkov and Takeva 1991).
Females usually breed as yearlings, with 1st-time
breeders often producing smaller litters than older females.
In Austria, yearling females weaned smaller litters (mean –
SD; 5.36 – 1.86 young/litter) than older mothers (6.8 – 1.72
young/litter—Huber et al. 1999). However, early-breeding
females also produced larger litters than later-breeding
females (Huber et al. 2001). Large litters are nursed longer
than smaller ones, with lactation in one season affecting
estrous delay in the next (Huber et al. 1999). Duration of
lactation varied from 22 to 52 days (Millesi et al. 1999a;
Aschauer et al. 2006) and 45 to 61 days (Huber et al. 2001;
Özkurt et al. 2005). According to Ružić (1978), lactation
typically continues after natal emergence, and lasts up to 6
weeks (Ružić-Petrov 1950). In Austria, onset of lactation
varied from late April to mid-May in accordance with
ovulation dates (Millesi et al. 1999a). Nonetheless, latereproductive females may nurse their offspring for a shorter
period to have ample time to prepare for hibernation
(Millesi et al. 2000).
ECOLOGY
Population characteristics.—Spermophilus citellus occurs
in loosely structured populations or colonies (Millesi et al.
1999b). In Austria, colonies occur mainly in isolated habitat
fragments, characteristic of relict populations (Hoffmann et
al. 2003b). Population densities may be quite variable, and
in low-density populations with few males, a female may
wait several days before being detected by a male (Millesi et
al. 2000). In 2 steppe areas of Hungary, population densities
varied from 15 to 55 and 50 to 90 individuals/ha over the
same active season (Váczi et al. 2006). Densities between 18
and 48 individuals/ha for optimal and 5 and 14 individuals/
ha for mountainous habitats in Serbia (Ružić 1978), as well
as 41–68 reproductive individuals/ha in Austria (Millesi et
al. 1998), have been reported. In the Pannonian plain,
densities of about 30 individuals/ha are considered high
(Ružić-Petrov 1950). Reduced immigration and increasing
mortality caused a drastic decline from 61 to 6.3 individuals/
46(913)—Spermophilus citellus
MAMMALIAN SPECIES
ha within a few years in a suburban area north of Vienna,
Austria (Hoffmann et al. 2003a).
Spermophilus citellus exhibits a remarkable plasticity in
life-history adaptations (Hoffmann 2002). Individuals can
live for up to 5 reproductive seasons (Millesi et al. 2000).
Maximum life span is 4 years for males and 6 years for
females (Hoffmann et al. 2003a), but may be . 9 years in
captivity (Andjus et al. 2000). Disappearance rates during
the active season are severalfold higher than overwinter
mortality, and may lead to the complete loss of a sex and age
class (Millesi et al. 1999b). Sex ratios in natural populations
from Austria were male-biased (1.6:1.0) with 26 juvenile
males and 12 juvenile females (Strauss et al. 2007a), and on
average 30.75 adult males and 19.25 adult females over a 4year period (2.1:1.0—Millesi et al. 1998). Annual percentages of surviving juveniles from Austria were lower than
those of nonjuveniles. Age-specific survival of males also
was lower than that of females in each cohort (Hoffmann et
al. 2003a), with late-born juveniles experiencing reduced
survival to the next season (Millesi et al. 2000). Litter
emergence date and offspring weaning body mass do not
affect juvenile survival to yearling age (Huber et al. 2001),
but do influence juvenile reproductive output in the
following season (Huber et al. 1999). However, offspring
body mass at natal emergence is positively related to
overwinter survival in young. Preweaning mortality is lower
in heavier young, whereas postweaning mortality is unaffected by juvenile body mass (Huber et al. 2001). Body
condition at onset of hibernation has a strong influence on
overwinter survival, and is related to maternal effort
(Aschauer et al. 2006). A mother’s probability of surviving
to subsequent breeding period is not influenced by either
litter size or mean body mass of young at emergence (Huber
et al. 1999).
Space use.—Spermophilus citellus characteristically
inhabits short-grass steppe, pastures, and meadows
(natural or anthropogenic), with sporadic shrubs and trees,
from sea level up to 2,500 m (Fig. 4; Kryštufek 1999;
Hoffmann et al. 2003b; Kryštufek and Vohralı́k 2005). It
occurs in arid lowlands with sandy loam-loess humus and
alluvial-meadow soil types (Brinkmann 1951; Ružić 1978;
Koshev and Kocheva 2007). The species is absent from
annually plowed arable land as well as tall-grass meadows
(Kryštufek and Vohralı́k 2005). However, it may dwell in
field margins, farm tracks, edges of sand or gravel pits,
embankments, and other anthropogenic environments
(Gloger 1833; Straschil 1972; Hoffmann et al. 2008). The
species has developed a tolerance toward tall vegetation,
shrubs, and trees in the past decades (Ružić 1978;
Spitzenberger and Bauer 2001). In Bulgaria, it may be
found in localities with average annual temperatures
between 108C and 138C (Koshev and Kocheva 2007). In
Macedonia, it is associated with dry, warm, open places with
deep soil that are regularly grazed by domestic animals,
77
whereas it is absent from stony, eroded slopes, and lowlands
with a high groundwater level (Kryštufek 1993). In the
Czech Republic, the species does not depend on a specific
plant or vegetation assemblage (Matějů et al. 2011) nor does
it require a particular soil type (Janderková et al. 2011).
Dominant plants occurring in the habitat of S. citellus in the
Black Sea coast of Bulgaria are Andropogon ischaemum,
Artemisia absinthium, Bromus arvense, Convolvus arvensis,
Cynodon dactylon, Eragrostis pilosa, Erodium cicutarium,
Euphorbia rupestris, Festuca pseudovina, Filipendula
hexapetala, Galium verrum, Marrubium peregrinum,
Medicago orbicularis, M. lipulina, Papaver rhoes, Plantago
lanceolata, Poa angustifolia, Polygonum aviculare, Salvia
nemorosa, and Thymus marschallianus (Paspalev and Peshev
1957).
Individual squirrels usually move within 60–80 m from
their own burrows, but when searching for nutritious food,
may travel . 100 m (Ružić 1978). One of us (IEH) observed
home ranges exceeding 1 ha in adult males throughout the
active season, but typically home ranges cover between 0.1
and 0.4 ha, depending on reproductive condition, sex, age,
population density, and habitat attributes (Huber 1996;
Matějů 2008; Turrini et al. 2008). After emergence from
hibernation, adult males show little aggression or locomotion and have small home ranges (X̄ ¼ 0.05 ha, interquartile
range ¼ 0.30–0.07 ha). This changes with mating when
aggression, locomotion, and home ranges increase considerably (X̄ ¼ 0.17 ha, interquartile range ¼ 0.15–0.27 ha—
Millesi et al. 1998), although after the mating period, range
sizes decrease again (Millesi et al. 2002), and do not differ
from female home ranges (Turrini et al. 2008). In a nearly
natural habitat, mean (– SD) adult home ranges were 0.435
ha (– 0.387 ha) for males and 0.330 ha (– 0.300 ha) for
females. Minimum home-range span in juveniles was 71 m
and in nonjuveniles 39 m, whereas maximum home-range
span in juveniles was 338 m and in nonjuveniles 203 m
(Turrini et al. 2008).
Dispersal starts about 30–40 days after natal emergence.
Juveniles begin to depart from their natal sites at 9 weeks of
age, and both sexes cover similar linear distances (up to 350
m—Hoffmann et al. 2004). Juvenile males move faster and
incur in a higher risk of predation than females when leaving
their natal home range (Hoffmann et al. 2004). According to
Sutherland et al. (2000), allometric relationships between
body mass and dispersal distance predict distances of , 1
km. Hence, dispersal is possible if the population is growing
and environments are suitable (Hulová and Sedláček 2008).
In a nearly natural habitat in Austria, a yearling male
traveled at least 750 m (Turrini et al. 2008).
Spermophilus citellus constructs and maintains simple
and elaborate burrows by scratch-digging (Lagaria and
Youlatos 2006). Burrows may be permanent (with a nest) or
temporary; the former are deeper. Burrows are located
mainly in open areas to allow good visibility, but depending
78
MAMMALIAN SPECIES
46(913)—Spermophilus citellus
Fig. 4.—Habitats commonly occupied by Spermophilus citellus in portions of its range: A, Romania, Iasi County, Osoi, elevation 140 m; B,
Macedonia, Mt. Jakupica, Gorno Begovo, elevation 2,000 m; C, Macedonia, Valandovo, elevation 150 m; D, Czech Republic, Mladá
Boleslav, elevation 205 m. Photographs courtesy of B. Kryštufek (A) and A. Kryštufek (B–D).
on habitat attributes and soil quality, burrows also occur
under shrubs (Kryštufek and Vohralı́k 2005), grapevines
(Hoffmann et al. 2008), or rocks (Calinescu 1934; Brinkmann 1951). When scratch-digging new or excavating
collapsed tunnels, S. citellus loosens the soil with forefeet
and incisors, scratches backwards, and uses the hind feet to
remove the material that accumulates under it during
digging (Ružić 1978; Lagaria and Youlatos 2006; Kley and
Kearney 2007). Individuals inhabit permanent burrow
systems with typically 1 chamber used for hibernation,
lactation, sleep, copulation, protection of food, and shortterm retreat (Ružić 1978; Lagaria and Youlatos 2006). Most
shelter burrows consist of blind-ending tubes without a nest,
but may be converted into permanent burrows, with number
and length of branches increasing with use of the burrow
(Ružić 1978). Each burrow system possesses 1–5 entrances
(5–10 cm wide) with up to 6 tunnels that vary in length from
0.5 to 4.5 m, reaching a maximal depth of 2 m (Brinkmann
1951; Ružić 1978). Trodden trails in the vegetation cover
connect burrow entrances on the surface (Brinkmann 1951).
Prior to hibernation, the inhabitant plugs the entrance with
soil and digs a blind-ending side branch (Ružić 1978). When
emerging in spring, the squirrel either opens the original
entrance or digs through a side branch (Ružić 1978), both
resulting in soil mounds at the entrance (Brinkmann 1951).
The 16- to 25-cm-wide nesting chamber is either the
deepest part of the burrow system (Ružić 1978) or is situated
higher than the entry tunnel to protect against floods
(Brinkmann 1951). If present, a 2nd chamber is used as a
latrine (Ružić 1978) and plugged with soil when filled
(Brinkmann 1951). Nesting material consists primarily of
grasses (Brinkmann 1951; Ružić 1978; Gedeon et al. 2010).
46(913)—Spermophilus citellus
MAMMALIAN SPECIES
Fig. 5.—An adult Spermophilus citellus from calcareous grassland
in Perchtoldsdorf, Lower Austria, elevation 300 m, feeding on sage
flowers (Salvia) on 30 June 2007. Used with permission of the
photographer C. J. Böswarth.
In Hungary, S. citellus preferred F. pseudovina versus
Bothriochloa ischaemum under laboratory conditions, with
fresh F. pseudovina providing flexible material that allowed
squirrels to construct nests with better insulation (Gedeon et
al. 2010). Common plants in nesting material in northern
Serbia were A. ischaemum, C. dactylon, Festuca valesiaca,
and Poa bulbosa (Ružić-Petrov 1950).
Diets.—Spermophilus citellus is predominantly
herbivorous, consuming green leaves, flowers, seeds, roots,
and shoots, but also may include arthropods in its diet (Fig.
5). Specimens from Moldavia (419 stomachs) and Romania
(650 pouches) contained 194 plant species from 45 families
(Dănilă 1984). Poaceae, Fabaceae, and Asteraceae together
constituted 33–100% of the plant diet (Dănilă 1984).
Squirrels in a recreation area in Austria foraged up to 75%
on dandelion (Taraxacum officinale) and switched to 50%
clover (Trifolium) as it became abundant. Dandelion and
clover species contain higher amounts of water, calcium, and
magnesium than the less-preferred ryegrass (Lolium
perenne—Pieta 1997). Thirty-one plants were identified in
northern Serbia (Ružić-Petrov 1950) and 38 in southeastern
Romania as part of its diet (Popescu 1972). In northern
Serbia, S. citellus consumed green parts (23 species of
plants), flowers (9 species), seeds (17 species), and
underground parts (5 species—Ružić-Petrov 1950) of
plants. When available, the species also feeds on
agricultural crops (seedlings, grains, fruits, and storage
organs—Ružić 1978; Dănilă 1984; Turrini et al. 2008). In
northern Serbia insects occurred in 13.4% of the stomachs of
S. citellus (Ružić-Petrov 1950; Ružić 1978), whereas in the
Czech Republic insects occurred in 33–66% of the stomachs
of pregnant females and 20% of adult males (Grulich 1960).
Vertebrates (i.e., young northern white-breasted hedgehogs
[Erinaceus roumanicus], common voles [Microtus arvalis],
79
house mice [Mus musculus], common shrews [Sorex araneus],
European mole [Talpa europaea], and eggs of groundnesting birds) are occasionally consumed by S. citellus
(Matějů et al. 2010a). The species has not been observed
caching food prior to hibernation, apparently relying
completely on stored body fat (Millesi et al. 1999b).
Young squirrels begin to feed on grasses and forbs soon
after emergence from their natal burrows (Huber et al.
2001). Nutritional manipulation in captive squirrels resulted
in rapid gain in body mass in juvenile males, but the specific
nutritional factors did not affect total body mass during the
study period (Strauss et al. 2007a).
Diseases and parasites.—Studies of coccidian parasites in
Spermophilus citellus are scanty. Three species of Eimeria
were observed in 14 specimens of S. citellus from Bulgaria
(prevalence in parentheses): E. citelli (80%), E.
callospermophili (70%), and E. cynomysis (35%—Wilber et
al. 1998; Golemansky and Koshev 2007). E. citelli produces
catharal enteritis in the small and large intestines of infected
S. citellus (Golemansky and Koshev 2007). Six specimens
from different localities in Bulgaria also contained Klossia
(Golemansky and Koshev 2009). A cytomegalovirus strain
was recovered from the submaxillary glands of healthy fullgrown S. citellus in Romania (Diosi et al. 1967). A new
herpesvirus recovered from the kidneys of mature S. citellus
produced an effect in tissue culture cells resembling that of
herpesviruses (Diosi et al. 1975). Hall (1916) described the
following 3 nematode species as parasites of S. citellus:
Oxyuris obvelata, Physaloptera citilli, and Trichuris leporis.
Other internal parasites may include Hymenolepis fraternal
and Moniliformis moniliformis (Matějů et al. 2010a). The
following ectoparasites were detected in nests of S. citellus:
ticks (Ixodes laguri), mites (Haemogamassus citelli and
Hirstionyssus criceti), and fleas (Neopsylla setosa,
Citellophilus simplex, C. orientalis, C. assimilis, and C.
agyrtes—Matějů et al. 2010a).
Interspecific interactions.—Predators of Spermophilus
citellus include black kite (Milvus migrans), falcons (saker
falcon [Falco cherrug], common kestrel [F. tinnunculus], and
peregrine falcon [F. peregrinus]), eagles (greater spotted
eagle [Aquila clanga], eastern imperial eagle [A. heliaca],
tawny eagle [A. rapax], booted eagle [Hieraaetus pennatus]),
hawks (northern goshawk [Accipiter gentilis] and Eurasian
sparrowhawk [A. nisus]), harriers (western marsh harrier
[Circus aeruginosus], hen harrier [C. cyaneus], and
Montagu’s harrier [C. pygargus]), common buzzards
(Buteo buteo), great bustards (Otis tarda), weasels (ermine
[Mustela erminea], steppe polecat [M. eversmanii], least
weasel [M. nivalis], and European polecat [M. putorius]),
marbled polecats (Vormela peregusna), red foxes (Vulpes
vulpes), beech martens (Martes foina), Eurasian magpies
(Pica pica), carrion crows (Corvus corone), and feral
domestic cats (Felis catus—Grulich 1960; Ružić 1978;
Millesi et al. 1999b; Hoffmann et al. 2004; Biró et al. 2005;
MAMMALIAN SPECIES
80
Lanszki 2005; Adamec et al. 2006; Hapl et al. 2006; Hulová
and Sedláček 2008; Matějů et al. 2010a). Low abundance of
S. citellus apparently caused a decline of imperial and tawny
eagles, saker falcons, and steppe polecats in Bulgaria,
Romania, Ukraine, and Slovakia (Adamec et al. 2006;
Matějů et al. 2010a). S. citellus is believed to avoid predation
by blocking its burrow tunnels with sand when entering and
leaving (Hut and Scharff 1998). Koshev (2010) reports 3
types of interspecific aggressive behavior of S. citellus
toward different vertebrate species: Balkan green lizard
(Lacerta trilineata), rook (Corvus frugilegus), and least
weasel. In Serbia, burrows of S. citellus are used by beetles
of the families Tenebrionidae, Copridae, and Carabidae,
and by European toads (Bufo bufo—Ružić-Petrov 1950).
The coprophagous beetles Ontophagus vitulus and Aphodius
citellorum use excrement of S. citellus as food (Matějů et al.
2010a).
Miscellaneous.—Temperature data loggers implanted in
the abdominal cavity of Spermophilus citellus proved a
reliable technique in hibernation research (Hut et al. 2002a).
Light-sensitive radiocollar transmitters have been used to
measure daily patterns of light perceived by S. citellus in
natural conditions (Hut et al. 1999). In an assessment of
population density using distance sampling, the effective
strip width along a linear transect was estimated at about 60
m (Kryštufek et al. 2012).
BEHAVIOR
Grouping behavior.—Although Spermophilus citellus lives
in colonies, with individual home ranges overlapping
(Turrini et al. 2008), each individual beyond maternal care
inhabits its own burrow system, and consequently the
species cannot be regarded as truly social (Váczi et al. 2006).
Nonagonistic interactions between males and females
precede mating events, increasing from proestrus until
mating and decreasing again through the postmating
period. During mating, male aggression is primarily
composed of chases and fights, resulting in frequent
injuries. Aggression is intense and directed particularly
toward other adult males (80.4%), and less intense toward
females (8.2%) and nonreproductive yearlings (11.4%). After
mating, aggression is noninjurious, composed of chases and
displacements directed equally among ages and sexes
(Millesi et al. 1998). Similar results were reported by
Strauss et al. (2007b), with adult males directing most
attacks toward mature competitors and only a few against
nonreproductive yearlings. The communal use of focal areas
indicates that there are no distinct mating territories (Millesi
et al. 1998). Despite endogen ous compo nents,
environmental releasers are important for the expression
of male mating behavior; however, the physiological basis is
unclear (Millesi et al. 2002). Infanticide has not been
observed in S. citellus (Millesi et al. 1999a).
46(913)—Spermophilus citellus
Reproductive behavior.—Spermophilus citellus is a
polygynous species (Huber at al. 2002). Mating occurs
after a courtship period of a few days when a male interacts
regularly with a female (Millesi et al. 1998). Receptivity
begins before mating, with females tolerating genital
inspection and grooming by males (Millesi et al. 2000).
During the premating and mating periods, adult males begin
aboveground activities earlier than yearling males. However,
during the mating season adult males spend less time
foraging than yearling males (Everts et al. 2004). Females
rear offspring in litter burrows that are normally separate
from hibernacula. After weaning, each offspring takes over
a separate burrow (Huber et al. 2002). During the
postmating period, considerable digging behavior in both
reproductive and nonreproductive males is commonly
observed. Whereas digging behavior in nonreproductive
males is restricted to their own burrows, reproductive males
dig at both their nest burrows and litter burrows of their
former mates. Saving the female time and energy to invest
more in gestation and lactation has been considered as
paternal effort (Huber et al. 2002).
Communication.—Eight call types have been described in
Spermophilus citellus: 3 tonal (alarm call, scream, and
chatter) and 5 wideband (grunt, rapid grunt, snarl, chirr,
and pant) calls; alarm calls are the loudest and most
common (Koshev and Pandourski 2008; Matrosova et al.
2012). Alarm calls may last 65–152 ms and are tonal sounds
usually consisting of 2 different elements that can be joined
together or separated by an interval (mean – SD) of 6 – 3
ms. The 1st element, which may last 45–112 ms with a peak
frequency of 7,230–9,210 Hz, lacks modulation in
frequency, whereas the 2nd element, which may last 13–62
ms with a peak frequency of 9,300–14,550 Hz, is highly
frequency modulated (Schneiderová and Policht 2011a). In
Hungary, emission of alarm calls peaked in June when litters
emerged from natal burrows (Katona et al. 2002). Scent
marking is restricted to the mating season (Millesi et al.
1998).
Miscellaneous behavior.—Spermophilus citellus is a diurnal
species with a pronounced annual cycle of aboveground
activity (Everts et al. 2004). The onset of daily activity
apparently does not track either dawn or dusk. On average,
squirrels emerge from their burrows 3.9 h after civil twilight
at dawn, and retreat 3.2 h before civil twilight at dusk (Hut
et al. 1999; Everts et al. 2004). S. citellus is more active
during the morning hours (0900–1100 h) than at midday
(1200–1400 h) on sunny days, but not on cloudy days (Váczi
et al. 2006). Daily activity is centered around 1200 h and has
an average length of 8.8 h. Within this daily activity phase
animals are on average 4.7 h (53%) aboveground and 3.5 h
(74%) of that time is spent foraging (Everts et al. 2004). In
arid parts of southern Macedonia, individuals become
lethargic during the summer peak, when water content in
plants falls from 70% to 22.5% (Kryštufek and Vohralı́k
46(913)—Spermophilus citellus
MAMMALIAN SPECIES
81
days) hibernated longer than males (median ¼ 185 days),
yearling males (median ¼ 178 days), and juveniles (median ¼
191 days—Millesi et al. 1999b). During hibernation,
squirrels seem to lack the need for a functional circadian
system (Hut et al. 2002b). Hibernation terminates in early
spring, when temperatures constantly range above 08C
(Straschil 1972), and hence depends on altitude and latitude.
On the Black Sea coast of Bulgaria, the 1st active individuals
are reported on 18 March and mass emergence starts on 1
April (Peshev 1955). Emergence dates range from 15
February to 28 April in Austria (Millesi et al. 1999a; Millesi
and Hoffmann 2008), 2 to 12 March in the lowlands of
northern Serbia, and 6 to 24 April in the mountains of
eastern Serbia (Ružić-Petrov 1950). Timing patterns of
emergence resemble those of other Spermophilus, in which
adult males emerge first from hibernation, but contrarily,
immerge into hibernation later than adult females, followed
by yearlings and juveniles (Millesi et al. 1999a, 1999b;
Strauss et al. 2007b; Youlatos et al. 2007; Millesi and
Hoffmann 2008). Nonreproductive yearling males are able
to dedicate 1 complete active season to growth and
preparation for hibernation, which may result in improved
body condition at spring emergence and higher survival
rates (Strauss et al. 2007b). However, late-born juveniles
may have less time to grow and fatten for hibernation
(Millesi et al. 2000). Juveniles terminate aboveground
activity between 3 September and 22 October, with a
distinct drop in temperature preceding immergence of the
last squirrels (Straschil 1972; Millesi et al. 1999b; Millesi and
Hoffmann 2008).
GENETICS
Fig. 6.—A lactating female Spermophilus citellus from calcareous
grassland in Perchtoldsdorf, Lower Austria, elevation 300 m, in
bipedal vigilance on 19 June 2004. Used with permission of the
photographer C. J. Böswarth.
2005). During aboveground activity, vigilance and foraging
are the dominant behaviors in all periods for males and
females (Youlatos et al. 2007). Scanning the surroundings
for potential threat in a bipedal posture is a conspicuous and
typical behavior (Fig. 6). Time spent in bipedal vigilance
peaks subsequent to juvenile emergence, coinciding with
peaks in population density, numbers of predators and
alarm calls, and elevated stress load (Hoffmann 1995;
Brenner 2011).
Spermophilus citellus is an obligate hibernator. Adult
and yearling females commonly enter hibernation in August,
hence the time for molt and fattening is limited (Millesi et al.
2000). Duration of hibernation in an enclosed population
was on average shorter in males (127.8 days) than in females
(171.3 days—Hut et al. 2002a). The same was observed in a
natural population in Austria where females (median ¼ 228
Cytogenetics.—The diploid chromosome number (2n) in
Spermophilus citellus is 40. Traditionally, the autosomal set
has been reported to include 2 pairs of metacentric, 12 pairs
of submetacentric, and 5 pairs of acrocentric chromosomes,
therefore a fundamental number (FN) of 69 and a
fundamental number of autosomes (FNa) of 66 (Belcheva
and Peshev 1979; Zima and Král 1984; Özkurt et al. 2002,
2007; Mitsainas et al. 2008). There may be inconsistencies
involved in the interpretation of autosomes with tiny short
arms. Therefore, Özkurt et al. (2007) reported for European
Turkey a cytotype with FN ¼ 78, FNa ¼ 74. Mitsainas et al.
(2008) claimed that all autosomal pairs are biarmed. The X
chromosome can be biarmed or acrocentric, whereas the Y
chromosome is the smallest element, either biarmed (Zima
and Král 1984) or acrocentric (Özkurt et al. 2002). The
biarmed Y chromosome was reported only from Turkey
(Özkurt et al. 2007). Soldatović et al. (1984) suggested that
the acrocentric Y chromosome was derived from a biarmed
condition by deletion. One Bulgarian population is unique
in that members have a pericentric inversion involving the X
chromosome (Belcheva and Peshev 1979). The C-band
82
MAMMALIAN SPECIES
staining technique indicated that all autosomes, as well as
the X chromosome, possessed prominently stained
centromeres. Some pairs demonstrated additional
heterochromatic bands at different positions on the short
or long arms (6, 8, 9, and 15). The Y chromosome appeared
fully heterochromatic (Mitsainas et al. 2008).
Molecular genetics.—Kruckenhauser et al. (1999) used
DNA sequences of the mitochondrial cytochrome-b (Cytb)
and mitochondrial cytochrome-b (Cytb) and NADHdehydrogenase subunit 4 (ND4) genes from Spermophilus
citellus to revisit the phylogeny of the genus Marmota.
Harrison et al. (2003) used complete mitochondrial Cytb
sequences from Spermophilus and Cynomys to reconstruct
the phylogeny and evolutionary history of ground squirrels.
Divergence based on Cytb sequences suggests that S.
taurensis separated from S. citellus 2.5 million years ago
and that the ancestor of these 2 species diverged from S.
xanthoprymnus about 5 million years ago (Gündüz et al.
2007). Using Cytb gene sequences, Herron et al. (2004)
suggested that the name Spermophilus is appropriate for the
species included in the Old World clade of the genus
Spermophilus (S. citellus, S. dauricus, S. erythrogenys [redcheeked ground squirrel], S. fulvus [yellow ground squirrel],
S. major [russet ground squirrel], S. musicus [Caucasian
Mountain ground squirrel], S. pallidicauda [pallid ground
squirrel], S. pygmaeus [little ground squirrel], S. relictus
[relict ground squirrel], S. suslicus, and S. xanthoprymnus).
Based on parameters of DNA reassociation kinetics, the
genome size calculated for S. citellus was 3.07 pg
(Ginatulina et al. 1982). Three highly divergent
phylogenetic lineages (southern, northern, and Jakupica)
were recognized using 31 Cytb haplotypes from different
locations ranging from the Czech Republic to European
Turkey and beyond (Kryštufek et al. 2009). These lineages
presumably originated from independent Quaternary
refugia for steppic biota in southeastern Europe.
Haplotypes of the northern lineage were found on both
sides of the Danube River, and in both of the 2 main
geographical fragments of the species. The Jakupica lineage
is an isolate on a high plateau in central Macedonia. The
southern lineage diverged at about 0.58 million years ago,
whereas the northern and the Jakupica lineages separated at
about 0.3 million years ago (Kryštufek et al. 2009).
Variability in 25 nonmetric cranial traits retrieved 3 main
groups of populations (Kryštufek 1990) that concur with
phylogeographic groups.
Population genetics.—The first 6 microsatellite markers
for Spermophilus citellus (loci ST7, ST10, SB10, SC2, SC4,
and SX) were extracted from ethanol-stored tissue samples
from the tail to establish a partial genomic library (Hanslik
and Kruckenhauser 2000). Gondek et al. (2006) cross-tested
primer pairs from S. suslicus with 10 individuals of S. citellus
from Austria, obtaining positive amplification for 6 of 9 loci
(Ssu1, Ssu3, Ssu5, Ssu13, Ssu15, and Ssu16); significant
46(913)—Spermophilus citellus
deficit of heterozygotes occurred for loci Ssu1 and Ssu16,
although no deviation from Hardy–Weinberg equilibrium
was detected when analyzing larger numbers of individuals.
A total of 382 specimens of S. citellus from central Europe
were genotyped using microsatellite loci designed originally
for the alpine marmot (Marmota marmota; MS41, MS45,
and MS56), Idaho ground squirrel (Urocitellus brunneus;
IGS-1 and IGS-110b), and S. suslicus (Ssu1, Ssu5, Ssu7,
Ssu8, Ssu13, Ssu15, and Ssu16). Populations of S. citellus
were strongly differentiated, with high levels of inbreeding.
Coefficients of inbreeding were higher in populations from
the western range (Czech Republic and western Slovakia;
FIS ¼ 0.27–0.79) than those from the east (Hungary and
eastern Slovakia; F I S ¼ 0.060–0.119), whereas
interpopulation differentiation was similarly high in both
groups: FST ¼ 0.23 (west) and FST ¼ 0.25 (east). No evidence
was found for contemporary selection on major
histocompatibility genes (Řı́čanová et al. 2011). Another
assessment of 117 individuals from Austria, Hungary, and
Romania for 11 microsatellite loci revealed a high (23.4%)
proportion of private alleles, presumably the result of
disintegration of local populations that might have been
historically connected genetically (Ben Slimen et al. 2012).
CONSERVATION
Spermophilus citellus was considered an agricultural pest
during centuries when rural communities paid rewards for
killed specimens (Brinkmann 1951; Spitzenberger and Bauer
2001), and large-scale pest-control measures were implemented, for instance in northern Serbia (Ružić-Petrov 1950)
and Macedonia (Gradojević 1928). The species is ‘‘Critically
Endangered’’ in the northwestern portion of the range
(Koshev 2008). Serious declines have been reported from
many portions of the range, particularly in the Pannonian
Plain, with some marginal isolates becoming extinct during
the past century (e.g., Germany, Poland, and Croatia). The
1st decline was reported in the 1930s from the northwestern
portion of the range (Matějů et al. 2010a). In habitats of
northern Serbia, high densities of S. citellus declined from .
30 individuals/ha in the late 1940s to approximately 5
individuals/ha in the late 1960s. The decline was less
conspicious in high mountain pastures in eastern Serbia,
where densities dropped from , 22 individuals/ha in the
1940s to , 5 individuals/ha in the 1960s. In colonies with
low densities, individuals do not expose themselves any
longer and avoid vocal communication (Ružić 1979).
Although large, stable populations still exist in many parts
of the species’ range, fragmentation already seems to be
critical. Nonetheless, Ćosić et al. (2013) found that
populations in Vojvodina are highly fragmented, but their
genetic variation is still higher than in peripheral populations in Central Europe. In the cultural landscape that
dominates the distribution range, S. citellus relies on
46(913)—Spermophilus citellus
MAMMALIAN SPECIES
heterogeneous, extensively cultivated farmland (Hoffmann
2002); hence, numbers have declined with increased intensification of agriculture (Spitzenberger 2005). Abandonment
of tripartite crop rotation, afforestation, and cultivation of
fallows led to population declines in Saxonia and Silesia
(then Germany) as early as in the 1930s (Brinkmann 1951).
Presently, the main threats are habitat loss due to urban
sprawl and other construction activities (Hoffmann et al.
2003b), the transformation of steppe into arable land, and
the abandonment of grazing, resulting in tall-grass meadows
where S. citellus cannot survive (Kryštufek 1999; Coroiu et
al. 2008). In 2007, the majority (74%) of S. citellus in the
Czech Republic lived in airfields (Matějů et al. 2010a).
Persistence in Austria largely depends on dispersal and
recolonization among colonies (Hoffmann et al. 2003b).
Spermophilus citellus is currently listed as ‘‘Endangered’’
under the Bern Convention, Appendix II (Kryštufek 1999)
and is listed in the European program NATURA 2000
(Hulová and Sedláček 2008). The species is included in the
Red List of Threatened Species by the International Union
for Conservation of Nature and Natural Resources as
‘‘Vulnerable’’ (Coroiu et al. 2008). It also is protected by the
European Union Habitats and Species Directive, Annexes II
and IV (Kryštufek 1999). In the Czech Republic, where S.
citellus was still widespread in the early 1950s (Grulich
1960), 34 colonies remained by 2007, but only 5 colonies
included . 200 individuals each (Matějů et al. 2008, 2010a).
As a result, the species is included in the list of endangered
species (category: ‘‘Critically Endangered’’), and is thus
under strict legal protection (Zima and Anděra 1996). In
addition, an action plan for S. citellus has been developed in
the Czech Republic (Matějů et al. 2010a). Several conservation programs have attempted to reintroduce or translocate the species into suitable habitats without great success
(Hulová and Sedláček 2008; Matějů et al. 2010b), except in
Poland, where it is considered as successful (Coroiu et al.
2008; Matějů et al. 2010b, 2012). In Moldova, S. citellus is
rare in the steppe and meadow ecosystems and has been
included in the country’s Red Book (Teleuta et al. 2004). In
Slovakia, S. citellus uses areas managed by humans (e.g.,
airfields, golf courses, sport areas, and horse race courses)
when degradation of its original habitat occurs (Hapl et al.
2006). The State Nature Conservancy of the Slovak
Republic has conducted several transfers and reestablishments of S. citellus (Adamec et al. 2006). The species is
included in the Slovak National Red List as ‘‘Endangered’’
(Hapl et al. 2006). Turkey has not declared the species
protected, although the population size in Thrace is
decreasing to a very low level because of intensive land use
(Özkurt et al. 2005). In Bulgaria, the species is covered by
the Biological Diversity Act, as a species ‘‘requiring priority
conservation of its habitat’’ (Annex 3 to Art. 37—Stefanov
and Markova 2009).
83
Kryštufek et al. (2009) recommended that 3 phylogeographical lineages (southern, northern, and Jakupica) of S.
citellus should be regarded as independent units for
conservation. The Jakupica lineage is the smallest, being
restricted to mountain pastures (1,500–2,250 m altitude) in
the Jakupica–Karadjica mountain system of central Macedonia. The total area (884 ha) is fragmented and 94% of S.
citellus occur in 4 colonies. Densities (0.8–5.5 adults/ha) are
lower than elsewhere and the total population is estimated at
, 2,000 adult individuals (Kryštufek et al. 2012). In a field
experiment, Gedeon et al. (2012) found that squirrels
preferred angled artificial burrows (about 308), which
facilitated digging, and medium-height grass (X̄ ¼ 18 – SE
1.5 cm) with overhead protection by grasses as an important
component after a translocation of animals. Matějů et al.
(2012) found that a soft method of releasing (i.e., use of
artificial burrows or fences or both) is an essential
component of a successful reintroduction.
ACKNOWLEDGMENTS
We thank Ö. Özkurt, Y. Koshev, J. Matějů, and S.
Shilova for providing information on Spermophilus citellus.
C. Mlinar took the photographs of the skull. A. Kryštufek
and C. J. Böswarth generously provided photographs of live
animals and habitats occupied by the species. Two
anonymous reviewers provided valuable comments that
improved the manuscript.
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Associate Editors of this account were PAMELA OWEN and
ERIC RICKART. Editor was MEREDITH J. HAMILTON.